What Would Happen to the Trees and Lianas If Apes Disappeared?

What would happen to the trees and lianas if apes disappeared?

D AVID B EAUNE

Abstract Apes, like many frugivorous animals, are crucial extended to the lesser apes, the gibbons (Hylobatidae; allies for the reproduction of several fruiting tree species. McConkey & Chivers, ). The bonobo was the last of Almost all apes, however, including bonobos Pan paniscus, the three African great ape species to be discovered. It is en- are threatened with extinction. How will this affect tree demic to the Democratic Republic of Congo, south of the conservation? How can plants that are adapted to seed dis- Congo River, and its habitat does not overlap with that of persal by apes reproduce without their dispersal vectors? At either chimpanzees or gorillas. Bonobos are mainly frugi- LuiKotale, in an evergreen tropical forest of the Democratic vorous (% of feeding sessions), spending c. . hours Republic of Congo, the recruitment of  plant species in the per day swallowing seeds (Plate ), which they transport absence of seed dispersal was investigated under the par- over a relatively long distance (% .  m; mean . ental canopy, where a proportion of seeds fall without hori- km). An individual will disperse . t of seeds (. million zontal dissemination. Most bonobo-dispersed plant species seeds .  mm in length, excluding those such as Ficus spp. (%of species) were unable to self-recruit under the can- and Musanga cecropioides) in its lifetime (Beaune et al., opy. As % of the tree species (% of trees) at LuiKotale b). More than  plant species are dispersed by bonobos are dispersed by bonobos there is a risk of ecosystem decay through endozoochory (Beaune et al., b). Passed seeds and simplification (reduced biodiversity) if Pan paniscus germinate more rapidly, more successfully and with greater disappears from its natural range. The extinction of other post-dispersal survival than unpassed seeds (seeds embed- apes from their forests could have similar consequences. ded in faeces are involved in diplochory with dung beetles; The conservation of tree species, therefore, must encompass Beaune et al., a). In the forest of LuiKotale % of tree conservation of pollinators, seed dispersal vectors and other species and % of individual trees rely on bonobos for seed species that provide ecological services to the trees and other dispersal, and functional overlap between the bonobo and fruiting plants. other frugivorous animals appears to be low (Beaune et al., b,c). Keywords Africa, bonobo, Congo basin, ecosystem decay, The seed dispersal service provided by bonobos is of forest ecology, Pan paniscus, seed dispersal, zoochory particular interest as the species is categorized as Endangered on the IUCN Red List (Fruth et al., ), listed on CITES Appendix I (CITES, )andunder Class A in the African Convention on the Conservation of Nature and Natural Resources (OAU, ). The popu- Introduction lation is estimated to number ,–, (Fruth et al., ). The greatest threat to the bonobo is poaching for he conservation of a species is dependent upon the con- the commercial bushmeat trade but the species’ survival servation of those species that provide it with ecological T is also threatened by forest fragmentation and degra- services. The question of how the extinction of one species dation. Despite international protection and local taboos could affect others is particularly pertinent in the case of the bonobos are still killed in their natural habitats, including great apes (Hominidae: chimpanzee Pan troglodytes, bono- in protected areas such as Salonga National Park (Hart bo Pan paniscus, gorilla Gorilla gorilla and orang-utan et al., ). Pongo pygmaeus) because they play an important role as I assessed the ecological importance of bonobos for key dispersers of woody species (Wrangham et al., ; fruiting plants by investigating the ability of the plant com- Voysey et al., ; Gross-Camp & Kaplin, ; Beaune munity to recruit without horizontal seed dispersal (i.e. et al., a,b,c; Effiom et al., ). This can also be without bonobos and other seed dispersal vectors). The hy- pothesis is that without seed dispersal several plant species DAVID BEAUNE Department of Primatology, Max Planck Institute for for which apes are obligate seed dispersers would not re- Evolutionary Anthropology, Leipzig, Germany, and Laboratoire cruit under the parental tree because of density-dependent Biogéosciences, UMR CNRS 6282, Université de Bourgogne, Dijon, France E-mail [email protected] effects on the survival of seeds and seedlings. I also discuss – Received  May . Revision requested  July . how bonobos depend on trees in this plant animal Accepted  October . First published online  February . mutualism.

Oryx, 2015, 49(3), 442–446 © 2015 Fauna & Flora International doi:10.1017/S0030605314000878 Downloaded from https://www.cambridge.org/core. IP address: 170.106.40.139, on 23 Sep 2021 at 21:26:18, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605314000878 Trees and apes 443

by bonobos (Beaune et al., b) were investigated during May –June , following the methodology of Chapman & Chapman (). All seedlings (,  cm high), saplings (– cm high) and poles (.  cm high, ,  cm diameter at breast height, DBH) were censused in the parental crown area (i.e. the fruit-fall zone) of adult trees . cm DBH, with no conspecifics within  m of the fruit-fall zone. The presence of seeds under the parental crown was confirmed by observation of falling seeds during animal feeding sessions and/or visual assessment of seeds present (fragments and fresh seeds). Mean numbers of seedlings, saplings and poles were calculated from a mini- mum of five adult plants per species. We considered an PLATE 1 Bonobo Pan paniscus eating velvet tamarind fruits adult plant to be able to self-replace when the mean pole (Dialium sp.) and swallowing seeds at LuiKotale, Democratic production per plant was $ . To confirm that a species Republic of Congo. Photograph: David Beaune/LKBP. was able to recruit outside its fruit-fall zone, density of re- cruits was estimated across the total census area.

Results

Nineteen plant species (three liana and  tree species) were dispersed efficiently by bonobo (Table ). Three species considered to be autochorous (i.e. dispersed by a plant’sown means) were included in the assessment for comparison (see Beaune et al., b,c for characterization of seed dispersal). For each plant species some seeds were not dispersed horizontally and were found under the parental crown. During bonobo and monkey (Cercopithecus cephus ascanius, Cercopithecus mona wolﬁ, Lophocebus aterrimus)feedingses- sions broken branches and fruits with seeds (dropped or spat) from the  fruiting plants were observed on the ground. The autochorous species recruited, on average, more than one pole under the parents, thus fulfilling the criterion for self- replacement. In contrast, the fleshy-fruited species dispersed by bonobos did not recruit enough poles under parent plants for self-replacement, except for Drypetes sp. (Table , Fig. ). FIG. 1 Location of the study site at LuiKotale, in Salonga Although seedlings, saplings and poles were found under National Park, Democratic Republic of Congo. other tree species (in a total of . ha censused), most adults of zoochorous (i.e. dispersed by animals) species were not able Study site to self-replace without seed dispersal beyond the fruit-fall zone, despite the presence of a seed bank. Fieldwork took place at LuiKotale, at the south-western fringe of Salonga National Park, Democratic Republic of  Congo (Fig. ). The study site comprised .  km of pri- Discussion mary evergreen lowland tropical rain forest (for more infor- The frugivorous bonobo relies on the fruits of  plant spe- mation about the study site and previous research cies, which account for . % of their diet (Beaune et al., conducted there see Beaune et al., a,b,c, a,b,c,d,e). b). During certain months trees such as Dialium spp. can account for . % of the bonobo’s diet (Beaune et al.,  Methods d). How tree populations depend on the ecological services provided by bonobos is more difficult to assess. To assess seedling recruitment under the parent crown, ma- However, without seed dispersal, zoochoric plant species ture trees of  species previously observed to fruit (thus ex- normally dispersed by bonobo recruit insufficient young cluding males of dioecious species) and efficiently dispersed under the fruit-fall zone for self-replacement, despite

TABLE 1 Mean number of seedlings, saplings and poles found under the canopy of adult individuals of  tree and liana species in LuiKotale, Democratic Republic of Congo (Fig. ).

Mean recruitment Tree species1 (Family), limiting seed size2 (cm) No. of individuals Mean DBH (cm) Seedling Sapling Pole Autochory Hymenostegia mundungu (Caesalpiniaceae) 10 73.7 4.4 4.1 2.5 Scorodophloeus zenkeri (Caesalpiniaceae) 10 48.4 16.3 2 3.4 Strombosiopsis zenkeri (Olacaceae) 11 35.6 2 2.1 1.2 Zoochory with bonobo Pan paniscus Anonidium mannii (Annonaceae) ↔4 10 46.7 0.5 0.6 0.4 Blighia welwitschii (Sapindaceae) ↔2 5 62.8 0 0.2 0.4 Canarium schweinfurthii (Burseraceae) ↔1.2 5 109.4 0 0 0 Cissus dinklagei (Vitaceae) ↔1 5 0.8 0 0 Drypetes sp. (Euphorbiaceae) ↔1 10 30.9 0.7 1.9 2.6 Enantia olivacea (Annonaceae) ↔1 6 15.4 0 1.8 0.8 Ficus sp. (Moraceae) ø 0.1 7 0 0 0 Gambeya lacourtiana (Sapotaceae)↔ 1.9 10 92.2 1 0 0 Grewia oligoneura (Malvaceae) ↔2 6 38.4 0.2 0.3 0.3 Irvingia gabonensis (Irvingiaceae) ↔5 54 83.1 1.7 0.0 0 Irvingia grandifolia (Irvingiaceae) ↔5 10 110 0 0 0 Klainedoxa gabonensis (Irvingiaceae) ↔4 10 124.5 0 0 0 Landolphia forestiana (Apocynaceae) ↔1.2 5 0 0.2 0 Landolphia sp. (Apocynaceae) ↔1.2 5 0 5.6 0.4 Mammea africana (Guttiferae) ↔6 10 117.6 0.1 0.9 0 Manilkara yangambiensis (Sapotaceae) ↔0.9 10 40.4 0.6 0.2 0.1 Pancovia laurentii (Sapindaceae) ↔0.8 10 27 0.1 1 0.5 Parinari excelsa (Chrysobalanaceae) ↔2.3 10 113.1 19.8 0.1 0.1 Greenwayodendron suaveolens (Annonaceae) ø1 10 29 0.1 1.6 0.5

 Botanical nomenclature follows the African Plants Database v. .. ()  The limiting greatest seed width or digestive tract passage size, indicated as diameter (ø) or length (↔)

regular seed restocking by gravity (barochory without fulfil the seed dispersal role of the apes for certain fruiting zoochory/anemochory). This may be attributable to the plants, but less effectively because the seed handling process, incapacity of seeds to germinate without handling and/or the dispersal distance, the number of seeds disseminated, to higher mortality under the parental crown as a result and the secondary dispersal by dung beetles would not be of density-dependent effects (Janzen, ; Connell, ; equivalent. Without the bonobo more seeds would fall in Schupp, ; Beaune et al., c, a). Bush pigs the fruit-fall zone, increasing the seed bank and conse- Potamochoerus porcus, giant pouched rats Cricetomys quently seed mortality as a result of increased predation. emini and  other seed predators at LuiKotale were ob- A similar survey for elephant-dispersed plant species in served foraging seeds under parent plants, and reduced the absence of elephants yielded the same result: the trees seed survival under the parental canopy (Beaune et al., did not recruit sufficiently for self-replacement, and seed a,b, c). Herbivorous animals also reduced the sur- predation was not saturated (Beaune et al., e). Fruiting vival of seedlings, saplings and poles, in a density-dependent plants, especially species with small seeds and several effect occurring under the parent plant, where a higher den- dispersal vectors, could potentially survive an extinction sity of seeds attracts more predators. An alternative way of of the bonobo, but this needs to be investigated further. examining this would be to compare two botanical plots The seed dispersal service provided by bonobos could from the same forest block, with and without bonobo popu- be provided by other, smaller animals but without the lations, or the same plot with a before and after control im- same dispersal effectiveness (and with potential population pact assessment after bonobo extinction. However, this genetics effects on the plants). Unlike the bonobo- would pose ethical and logistical problems. Despite its lim- dispersed species, autochoric trees such as Hymenostegia itations the assessment presented here gives an indication of mundungu, Scorodophloeus zenkeri and Strombosiopsis the seed and recruitment mortality under the parental zenkeri are adapted to short dispersal distance and their crown of species adapted to zoochory. Other, smaller seed seeds probably contain antifeedant and other toxic dispersal vectors, such as monkeys, bats and birds, could compounds.

FIG. 2 Mean (±SE) recruitment of poles (,  cm DBH) under the parent crown for three autochorous species (HM, Hymenostegia mundungu; ScZ, Scorodophloeus zenkeri; StZ, Strombosiopsis zenkeri) and  species dispersed by bonobos Pan paniscus (AM, Anonidium mannii; BW, Blighia welwitschii; CS, Canarium schweinfurthii; CD, Cissus dinklagei; DS, Drypetes sp.; EO, Enantia olivacea; FS, Ficus sp.; GL, Gambeya lacourtiana; GO, Grewia oligoneura; GS, Greenwayodendron suaveolens; IG, Irvingia gabonensis; IGr, Irvingia grandifolia; KG, Klainedoxa gabonensis; LF, Landolphia forestiana; LS, Landolphia sp.; MA, Mammea africana; MY, Manilkara yangambiensis; PL, Pancovia laurentii; PE, Parinari excelsa) at LuiKotale (Fig. ). The dotted line is the threshold for self-replacement of the parent.

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